Topical N-acetyl-S-farnesyl-L-cysteine inhibits mouse skin inflammation, and unlike dexamethasone, its effects are restricted to the application site

Journal of Investigative Dermatology

Volumn 128, Issue 3, 2008, Pages 643-654

  Gordon, Joel S ^a   Wolanin, Peter M ^a   Gonzalez, Arnold V ^a   Fela, David A ^a   Sarngadharan, Gopal ^a   Rouzard, Karl ^a   Perez, Eduardo ^a   Stock, Jeffry B ^a,b   Stock, Maxwell B ^a,c  

^a Signum Biosciences   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; ARACHIDONIC ACID; DEXAMETHASONE; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; INDOMETACIN; MYELOPEROXIDASE; N ACETYL S FARNESYL L CYSTEINE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EAR; ENZYME ACTIVITY; ENZYME INHIBITION; EPIDERMIS HYPERPLASIA; HISTOCHEMISTRY; IN VIVO STUDY; MALE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; SKIN ALLERGY; SKIN INFLAMMATION; SKIN SENSITIZATION;

ACETYLCYSTEINE; ADMINISTRATION, TOPICAL; ANIMALS; ANIMALS, OUTBRED STRAINS; ANTI-INFLAMMATORY AGENTS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; DERMATITIS; DEXAMETHASONE; DISEASE MODELS, ANIMAL; EAR, EXTERNAL; EDEMA; ENZYME INHIBITORS; INDOMETHACIN; MALE; MICE; MICE, INBRED ICR; NEUTROPHILS; PEROXIDASE;

EID: 39149127566     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/sj.jid.5701061     Document Type: Article

References (81)

1. Abbinante-Nissen JM, Simpson LG, Leikauf GD (1995) Corticosteroids increase secretory leukocyte protease inhibitor transcript levels in airway epithelial cells. Am J Physiol 268:L601-6
2. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with Image. J Biophotonics Int 11:36-42
3. Ahmad M, Zhang Y, Zhang Y, Papharalambus C, Alexander RW (2002) Role of isoprenylcysteine carboxyl methyltransferase in tumor necrosis factor-alpha stimulation of expression of vascular cell adhesion molecule-1 in endothelial cells. Arterioscler Thromb Vasc Biol 22:759-64
4. Bargatze RF, Butcher EC (1993) Rapid G protein-regulated activation event involved in lymphocyte binding to high endothelial venules. J Exp Med 178:367-72
5. Beato M, Herrlich P, Schutz G (1995) Steroid hormone receptors: many actors in search of a plot. Cell 83:851-7
6. Belvisi MG, Brown TJ, Wicks S, Foster ML (2001a) New glucocorticosteroids with an improved therapeutic ratio? Pulm Pharmacol Ther 14:221-7
7. Belvisi MG, Wicks SL, Battram CH, Bottoms SE, Redford JE, Woodman P et al. (2001b) Therapeutic benefit of a dissociated glucocorticoid and the relevance of in vitro separation of transrepression from transactivation activity. J Immunol 166:1975-82
8. Bradley PP, Priebat DA, Christensen RD, Rothstein G (1982) Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78:206-9
9. Cacalano G, Lee J, Kikly K, Ryan AM, Pitts-Meek S, Hultgren B et al. (1994) Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265:682-4
10. Caldenhoven E, Liden J, Wissink S, Van de Stolpe A, Raaijmakers J, Koenderman L et al. (1995) Negative cross-talk between RelA and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids. Mol Endocrinol 9:401-12
11. Carlson RP, O'Neill-Davis L, Chang J, Lewis AJ (1985) Modulation of mouse ear edema by cyclooxygenase and lipoxygenase inhibitors and other pharmacologic agents. Agents Actions 17:197-204
12. Casey PJ, Solski PA, Der CJ, Buss JE (1989) p21ras is modified by a farnesyl isoprenoid. Proc Natl Acad Sci USA 86:8323-7
13. Cataisson C, Joseloff E, Murillas R, Wang A, Atwell C, Torgerson S et al. (2003) Activation of cutaneous protein kinase C alpha induces keratinocyte apoptosis and intraepidermal inflammation by independent signaling pathways. J Immunol 171:2703-13
14. Cataisson C, Pearson AJ, Torgerson S, Nedospasov SA, Yuspa SH (2005) Protein kinase C alpha-mediated chemotaxis of neutrophils requires NF-kappa B activity but is independent of TNF alpha signaling in mouse skin in vivo. J Immunol 174:1686-92
15. Cataisson C, Pearson AJ, Tsien MZ, Mascia F, Gao JL, Pastore S et al. (2006) CXCR2 ligands and G-CSF mediate PKCalpha-induced intraepidermal inflammation. J Clin Invest 116:2757-66
16. Clarke S (1988) Perspectives on the biological function and enzymology of protein carboxyl methylation reactions in eucaryotic and procaryotic cells. Adv Exp Med Biol 231:213-28
17. Coghlan MJ, Jacobson PB, Lane B, Nakane M, Lin CW, Elmore SW et al. (2003) A novel antiinflammatory maintains glucocorticoid efficacy with reduced side effects. Mol Endocrinol 17:860-9
18. Crowle AJ (1975) Delayed hypersensitivity in the mouse. Adv Immunol 20:197-264
19. De Young LM, Kheifets JB, Ballaron SJ, Young JM (1989) Edema and cell infiltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents. Agents Actions 26:335-41
20. Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR (1990) Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249:1266-72
21. Ding J, Lu DJ, Perez-Sala D, Ma YT, Maddox JF, Gilbert BA et al. (1994) Farnesyl-L-cysteine analogs can inhibit or initiate superoxide release by human neutrophils. J Biol Chem 269:16837-44
22. Dlugosz AA, Yuspa SH (1993) Coordinate changes in gene expression which mark the spinous to granular cell transition in epidermis are regulated by protein kinase C. J Cell Biol 120:217-25
23. Epstein WW, Lever D, Leining LM, Bruenger E, Rilling HC (1991) Quantitation of prenylcysteines by a selective cleavage reaction. Proc Natl Acad Sci USA 88:9668-70
24. Evans RM (1988) The steroid and thyroid hormone receptor superfamily. Science 240:889-95
25. Ferreira SH, Moncada S, Vane JR (1971) Indomethacin and aspirin abolish prostaglandin release from the spleen. Nat New Biol 231:237-9
26. Forsberg M, Druid P, Zheng L, Stendahl O, Sarndahl E (2003) Activation of Rac2 and Cdc42 on Fc and complement receptor ligation in human neutrophils. J Leukoc Biol 74:611-9
27. Garrigue JL, Nicolas JF, Fraginals R, Benezra C, Bour H, Schmitt D (1994) Optimization of the mouse ear swelling test for in vivo and in vitro studies of weak contact sensitizers. Contact Dermatitis 30:231-237
28. Graff G, Gamache DA, Brady MT, Spellman JM, Yanni JM (1998) Improved myeloperoxidase assay for quantitation of neutrophil influx in a rat model of endotoxin-induced uveitis. J Pharmacol Toxicol Methods 39:169-78
29. Griffiths RJ, Wood BE, Li S, Blackham A (1988) Pharmacological modification of 12-0-tetradecanoylphorbol-13-acetate induced inflammation and epidermal cell proliferation in mouse skin. Agents Actions 25:344-51
30. Gronemeyer H (1992) Control of transcription activation by steroid hormone receptors. FASEB J 6:2524-9
31. Gschwendt M, Kittstein W, Furstenberger G, Marks F (1984) The mouse ear edema: a quantitatively evaluable assay for tumor promoting compounds and for inhibitors of tumor promotion. Cancer Lett 25:177-85
32. Hancock JF, Magee AI, Childs JE, Marshall CJ (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167-77
33. Hara T, Saito Y, Hirai T, Nakamura K, Nakao K, Katsuki M et al. (2005) Deficiency of protein kinase Calpha in mice results in impairment of epidermal hyperplasia and enhancement of tumor formation in two-stage skin carcinogenesis. Cancer Res 65:7356-62
34. Huzoor-Akbar, Wang W, Kornhauser R, Volker C, Stock JB (1993) Protein prenylcysteine analog inhibits agonist-receptor-mediated signal transduction in human platelets. Proc Natl Acad Sci USA 90:868-72
35. Jansen AP, Dreckschmidt NE, Verwiebe EG, Wheeler DL, Oberley TD, Verma AK (2001) Relation of the induction of epidermal ornithine decarboxylase and hyperplasia to the different skin tumor-promotion susceptibilities of protein kinase C alpha, -delta and -epsilon transgenic mice. Int J Cancer 93:635-43
36. Jetten AM, George MA, Pettit GR, Herald CL, Rearick JI (1989) Action of phorbol esters, bryostatins, and retinoic acid on cholesterol sulfate synthesis: relation to the multistep process of differentiation in human epidermal keratinocytes. J Invest Dermatol 93:108-15
37. Jonat C, Rahmsdorf HJ, Park KK, Cato AC, Gebel S, Ponta H et al. (1990) Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell 62:1189-204
38. Kostenis E (2004) A glance at G-protein-coupled receptors for lipid mediators: a growing receptor family with remarkably diverse ligands. Pharmacol Ther 102:243-57
39. Kotyuk B, Raychaudhuri A, DiPasquale G (1993) Effect of anti-inflammatory compounds on edema formation and myeloperoxidase activity in the arachidonic acid-induced ear model in the mouse. Agents Actions 39:C46-8
40. Kulke R, Bornscheuer E, Schluter C, Bartels J, Rowert J, Sticherling M et al. (1998) The CXC receptor 2 is overexpressed in psoriatic epidermis. J Invest Dermatol 110:90-4
41. Laudanna C, Campbell JJ, Butcher EC (1996) Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271:981-3
42. Levine SJ, Benfield T, Shelhamer JH (1996) Corticosteroids induce intracellular interleukin-1 receptor antagonist type I expression by a human airway epithelial cell line. Am J Respir Cell Mol Biol 15:245-51
43. Liu WS, Heckman CA (1998) The sevenfold way of PKC regulation. Cell Signal 10:529-42
44. Lu JY, Hofmann SL (2006) Thematic review series: lipid posttranslational modifications. Lysosomal metabolism of lipid-modified proteins. J Lipid Res 47:1352-7
45. Lucibello FC, Slater EP, Jooss KU, Beato M, Muller R (1990) Mutual transrepression of Fos and the glucocorticoid receptor: involvement of a functional domain in Fos which is absent in FosB. EMBO J 9: 2827-34
46. Mackie AE, Bye A (2000) The relationship between systemic exposure to fluticasone propionate and cortisol reduction in healthy male volunteers. Clin Pharmacokinet 39(Suppl 1):47-54
47. Michaelidou AS, Hadjipavlou-Litina D (2005) Nonsteroidal anti-inflammatory drugs (NSAIDs): a comparative QSAR study. Chem Rev 105: 3235-3271
48. Mukaida N, Morita M, Ishikawa Y, Rice N, Okamoto S, Kasahara T et al. (1994) Novel mechanism of glucocorticoid-mediated gene repression. Nuclear factor-kappa B is target for glucocorticoid-mediated interleukin 8 gene repression. J Biol Chem 269:13289-95
49. Opas EE, Bonney RJ, Humes JL (1985) Prostaglandin and leukotriene synthesis in mouse ears inflamed by arachidonic acid. J Invest Dermatol 84:253-6
50. Oppenheim JJ, Zachariae CO, Mukaida N, Matsushima K (1991) Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol 9:617-48
51. Philips MR, Pillinger MH, Staud R, Volker C, Rosenfeld MG, Weissmann G et al. (1993) Carboxyl methylation of Ras-related proteins during signal transduction in neutrophils. Science 259:977-80
52. Rao TS, Currie JL, Shaffer AF, Isakson PC (1993) Comparative evaluation of arachidonic acid (AA)- and tetradecanoylphorbol acetate (TPA)-induced dermal inflammation. Inflammation 17:723-41
53. Ray A, Prefontaine KE (1994) Physical association and functional antagonism between the p65 subunit of transcription factor NF-kappa B and the glucocorticoid receptor. Proc Natl Acad Sci USA 91:752-6
54. Reichardt HM, Tuckermann JP, Gottlicher M, Vujic M, Weih F, Angel P et al. (2001) Repression of inflammatory responses in the absence of DNA binding by the glucocorticoid receptor. EMBO J 20:7168-73
55. Reiss Y, Goldstein JL, Seabra MC, Casey PJ, Brown MS (1990) Inhibition of purified p21ras farnesyl:protein transferase by Cys-AAX tetrapeptides. Cell 62:81-8
56. Reynolds NJ, McCombie SW, Shankar BB, Bishop WR, Fisher GJ (1997) SCH 47112, a novel staurosporine derivative, inhibits 12-O-tetradecanoylphorbol-13-acetate-induced inflammation and epidermal hyperplasia in hairless mouse skin. Arch Dermatol Res 289:540-6
57. Saint-Mezard P, Krasteva M, Chavagnac C, Bosset S, Akiba H, Kehren J et al. (2003) Afferent and efferent phases of allergic contact dermatitis (ACD) can be induced after a single skin contact with haptens: evidence using a mouse model of primary ACD. J Invest Dermatol 120:641-7
58. Santangelo F (2003) Intracellular thiol concentration modulating inflammatory response: influence on the regulation of cell functions through cysteine prodrug approach. Curr Med Chem 10:2599-610
59. Schacke H, Schottelius A, Docke WD, Strehlke P, Jaroch S, Schmees N et al. (2004) Dissociation of transactivation from transrepression by a selective glucocorticoid receptor agonist leads to separation of therapeutic effects from side effects. Proc Natl Acad Sci USA 101:227-32
60. Schafer-Korting M, Kleuser B, Ahmed M, Holtje HD, Korting HC (2005) Glucocorticoids for human skin: new aspects of the mechanism of action. Skin Pharmacol Physiol 18:103-14
61. Scheer A, Gierschik P (1993) Farnesylcysteine analogues inhibit chemotactic peptide receptor-mediated G-protein activation in human HL-60 granulocyte membranes. FEBS Lett 319:110-4
62. Schottelius AJ, Giesen C, Asadullah K, Fierro IM, Colgan SP, Bauman J et al. (2002) An aspirin-triggered lipoxin A4 stable analog displays a unique topical anti-inflammatory profile. J Immunol 169:7063-70
63. Schüle R, Rangarajan P, Kliewer S, Ransone LJ, Bolado J, Yang N et al. (1990) Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell 62:1217-26
64. Smith JB, Willis AL (1971) Aspirin selectively inhibits prostaglandin production in human platelets. Nat New Biol 231:235-7
65. Sousa AR, Lane SJ, Nakhosteen JA, Lee TH, Poston RN (1996) Expression of interleukin-1 beta (IL-1beta) and interleukin-1 receptor antagonist (IL-1ra) on asthmatic bronchial epithelium. Am J Respir Crit Care Med 154:1061-6
66. Stimmel JB, Deschenes RJ, Volker C, Stock J, Clarke S (1990) Evidence for an S-farnesylcysteine methyl ester at the carboxyl terminus of the Saccharomyces cerevisiae RAS2 protein. Biochemistry (Mosc) 29:9651-9
67. Tramposch KM (1999) Skin inflamation. In In vivo Models of Inflammation. (Morgan DW, Marshall LA eds), Birkhäuser Verlag: Basel, pp 179-204
68. Van Arman CG (1974) Anti-inflammatory drugs. Clin Pharmacol Ther 16:900-4
69. Vane JR (1971) Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 231:232-5
70. Vayssiere BM, Dupont S, Choquart A, Petit F, Garcia T, Marchandeau C et al. (1997) Synthetic glucocorticoids that dissociate transactivation and AP-1 transrepression exhibit antiinflammatory activity in vivo. Mol Endocrinol 11:1245-55
71. Volker C, Lane P, Kwee C, Johnson M, Stock J (1991a) A single activity carboxyl methylates both farnesyl and geranylgeranyl cysteine residues. FEBS Lett 295:189-94
72. Volker C, Miller RA, Stock JB (1990) S-Farnesylcysteine methyltransferase in bovine brain. Methods 1:283-7
73. Volker C, Miller RA, McCleary WR, Rao A, Poenie M, Backer JM et al. (1991b) Effects of farnesylcysteine analogs on protein carboxyl methylation and signal transduction. J Biol Chem 266:21515-22
74. Volker CR (1995) Carboxyl methylation at C-terminal S-prenylcysteine residues. Department of Chemistry, Princeton University PhD Thesis. 571pp
75. Wang HQ, Smart RC (1999) Overexpression of protein kinase C-alpha in the epidermis of transgenic mice results in striking alterations in phorbol ester-induced inflammation and COX-2, MIP-2 and TNF-alpha expression but not tumor promotion. J Cell Sci 112(Part 20): 3497-506
76. Wu D, LaRosa GJ, Simon MI (1993) G protein-coupled signal transduction pathways for interleukin-8. Science 261:101-3
77. Yang-Yen HF, Chambard JC, Sun YL, Smeal T, Schmidt TJ, Drouin J et al. (1990) Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62:1205-15
78. Young JM, Spires DA, Bedord CJ, Wagner B, Ballaron SJ, De Young LM (1984) The mouse ear inflammatory response to topical arachidonic acid. J Invest Dermatol 82:367-71
79. Young JM, Wagner BM, Spires DA (1983) Tachyphylaxis in 12-O-tetradecanoylphorbol acetate- and arachidonic acid-induced ear edema. J Invest Dermatol 80:48-52
80. Zhang L, Tschantz WR, Casey PJ (1997a) Isolation and characterization of a prenylcysteine lyase from bovine brain. J Biol Chem 272:23354-9
81. Zhang Z, Zimonjic DB, Popescu NC, Wang N, Gerhard DS, Stone EM et al. (1997b) Human uteroglobin gene: structure, subchromosomal localization, and polymorphism. DNA Cell Biol 16:73-83